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Susceptibility of Candida Glabrata Biofilms to Echinocandins: Alterations in the Matrix Composition

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Susceptibility of Candida Glabrata Biofilms to Echinocandins: Alterations in the Matrix Composition BIOFOULING, 2018 VOL. 34, NO. 5, 569–578 https://doi.org/10.1080/08927014.2018.1472244 Susceptibility of Candida glabrata biofilms to echinocandins: alterations in the matrix composition Célia F. Rodrigues , Maria Elisa Rodrigues and Mariana Henriques CEB, Centre of Biological Engineering, LIBRO – Laboratório de Investigação em Biofilmes Rosário Oliveira, University of Minho, Braga, Portugal ABSTRACT ARTICLE HISTORY Candidiases are the most recurrent fungal infections, especially among immunosuppressed patients. Received 9 January 2018 Although Candida albicans is still the most widespread isolated species, non-Candida albicans Accepted 28 April 2018 Candida species have been increasing. The goal of this work was to determine the susceptibility of KEYWORDS C. glabrata biofilms to echinocandins and to evaluate their effect on the biofilm matrix composition, Candida glabrata; comparing the results with other Candida species. Drug susceptibilities were assessed through echinocandin; biofilm; the determination of minimum inhibitory concentration (MIC), minimum fungicidal concentration matrix; antifungal drug; (MFC) and minimum biofilm eradication concentration (MBEC) of caspofungin (Csf) and micafugin resistance (Mcf). The β-1,3 glucans content of the matrices was assessed after contact with the drugs. The data suggest that, generally, after contact with echinocandins, the concentration of β-1,3 glucans increased. These adjustments in the matrix composition of C. glabrata biofilms and the chemical differences between Csf and Mcf, seem responsible and may determine the effectivity of the drug responses. Introduction of exopolymeric compounds secreted by sessile cells, with all providing protection against environmental challenges Infections caused by members of the genus Candida (Pierce et al. 2017). Infections caused by biofilms are com- (candidiasis) have been increasing in recent decades and plicated due to inducible gene networks encoding different becoming more difficult to eradicate. There are about 15 proteins that confer tolerance or resistance to many of the differentCandida species that cause infections in humans, available antifungal drugs (Ramage et al. 2012). and Candida glabrata is one of the most common (Pappas Chemically, echinocandins are cyclic lipo-hexapeptides 2006; Pappas et al. 2015). Candidiasis generally occurs due with modified N-linked acyl lipid side chains (Chang to the unbalanced use of immunosuppressive drugs, broad et al. 2017), biosynthesised by diverse members of the spectrum antibiotics and the widespread use of indwell- Ascomycota (fungi) on non-ribosomal peptide synthase ing medical devices, but also to the growth of immuno- complexes (Emri et al. 2013). The first echinocandin with genic diseases, the upsurge of endocrine disorders, and antimycotic activity was discovered in the 1970s, and the ageing and the increase in the patient population since, over 20 natural echinocandins have been isolated (Douglas 2003; Li et al. 2007; Garcia-Cuesta et al. 2014; (Emri et al. 2013). By disturbing fungal cell wall synthe- Silva et al. 2017). Each Candida species has distinctive sis through a non-competitive inhibition of β-1,3-glucan virulence factors, antifungal susceptibilities, and defined synthesis, these drugs weaken the cell wall, break down epidemiologies (Pappas et al. 2015). The aptitude of these the cellular integrity and, finally, induce cell lysis (Debono organisms to form biofilms is a specific virulence feature and Gordee 1994; Perlin et al. 2007). Due to this mech- which allows tissue attachment following infection of the anism of action the echinocandins (which include anid- host (McCall and Edgerton 2017). Biofilms are commu- ulafungin, caspofungin and micafungin) are generally nities of microorganisms embedded in an extracellular well tolerated, avoiding the overlapping toxicities and matrix (Costerton et al. 1995; Donlan and Costerton drug–drug interactions with mammalian cells which are 2002), which confers significant resistance to antifungal observed with the azoles and the polyenes (Wiederhold therapy and intense host immune responses (Fonseca et and Lewis 2003; Wiederhold et al. 2007; Chang et al. al. 2014; Rodrigues et al. 2014). This matrix is composed 2017). The high clinical efficacy in the non-neutropenic CONTACT Mariana Henriques [email protected] © 2018 Informa UK Limited, trading as Taylor & Francis Group 570 C. F. RODRIGUES ET AL. patient population, in patients with moderate to severe cavity (C. glabrata AE2 and D1), urinary tract (C. glabrata illness, and in patients with pre-azole exposure (Pappas 562123 and 513100), vaginal tract (C. glabrata 534784 and et al. 2015; Perlin 2015b), resulted in echinocandins being 585626); four reference strains were from the American recommended as the first-line antifungal agents to treat Type Culture Collection (C. glabrata ATCC2001, C. invasive candidiasis, especially Candida glabrata, due albicans SC5314 (ATCCMYA2876), C. parapsilosis to its innate high azole resistance (Perlin 2007; Pappas ATCC22019 and C. tropicalis ATCC750). The identity of et al. 2015). Although these antifungal drugs are active all isolates was confirmed using CHROMagar Candida against most important Candida species, in which they (CHROMagar, Paris, France) and by PCR-based sequenc- display in vitro fungicidal activity (Barchiesi et al. 2005), ing using specific primers (ITS1 and ITS4) against the in critically ill patients it is recognised that the achieve- 5.8s subunit gene reference. Genomic DNA was extracted ment of their pharmacodynamic and pharmacokinetic following previously described procedures (Williams et al. targets show a large inter-individual variability (Chang 1995). The PCR products were sequenced using the ABI- et al. 2017). In Europe, micafungin (Mcf) is approved for PRISM Big Dye terminator cycle sequencing kit (Perkin use in paediatric patients of any age including neonates, Elmer, Applied Biosystems, Warrington, UK). while caspofungin (Csf) is approved for use in paediat- ric patients ≥ 1 year old, since there are insufficient data Growth conditions regarding its use in those <1 year old (Tragiannidis et al. 2012; Viscoli et al. 2014). The use of Csf and Mcf is lim- For each experiment, strains were subcultured on ited by the necessity for a once-daily intravenous dosage Sabouraud dextrose agar (SDA) (Merck, Darmstadt, regimen, lack of an oral formulation and a limited spec- Germany) for 24 h at 37°C. Cells were then inoculated in trum (Barchiesi et al. 2005; Pappas et al. 2015; McCarty Sabouraud dextrose broth (SDB) (Merck) and incubated and Pappas 2016), but both echinocandins still show very for 18 h at 37°C, under agitation at 120 rpm. After incu- good in vitro activity against clinically relevant isolates of bation, the cells were harvested by centrifugation, 3,000 g Candida species (Pappas et al. 2007; Spreghini et al. 2012; for 10 min, at 4°C and washed twice with phosphate Kohno et al. 2013; Perlin 2015a; Chapman et al. 2017). In buffer saline (PBS, 0.1 M, pH=7.5; NaCl 0.8%, KCl 0.02%, trials involving adult and paediatric patients with invasive K2HPO4 0.02%, NaHPO4.12H2O 0.285%). Pellets were and oesophageal candidiasis, Mcf has been shown to be then suspended in RPMI-1640 (pH=7, Sigma-Aldrich, non-inferior to intravenous Csf, intravenous fluconazole St Louis, MO, USA) and the cellular density was adjusted or liposomal amphotericin B. The tolerability profile of to 1×105 cells ml−1, using a Neubauer counting chamber. Csf and Mcf are, in general, similar to fluconazole and are better tolerated than liposomal amphotericin B or oral Antifungal drugs itraconazole (Scott 2012). The biofilm matrices ofCandida species have a strong Csf and Mcf were kindly provided by MSD® and Astellas®, net of exopolymers, providing protection against physi- respectively. Aliquots of 5,000 mg l−1 were prepared using cal and chemical environmental attack, such as by drugs. dimethyl-sulfoxide (DMSO). The final concentrations These polymers make it difficult for drugs to diffuse into used were prepared with RPMI-1640 (Sigma-Aldrich) the biofilm cells, which make the biofilms recalcitrant to for both drugs. antifungals (Al-Fattani and Douglas 2004; Rodrigues, Gonçalves et al. 2017; Dominguez et al. 2018). Hence, Antifungal susceptibility tests the goal of this work was to evaluate seven C. glabrata isolates, by comparison with C. albicans, C. parapsilosis All the antifungal susceptibility tests were performed and C. tropicalis, regarding their susceptibility in the using the microdilution method, in accordance to the planktonic and biofilm form to Csf and Mcf, and the bio- European Committee on Antimicrobial Susceptibility chemical variations induced in the composition of the Testing (EUCAST) guidelines (EUCAST [date unknown]; matrices after the drug exposure, in order to relate these Arendrup et al. 2008). matrix variations with drug effectiveness. Minimum inhibitory concentrations (MICs) Material and methods The inoculum was prepared by suspending five distinct colonies, ≥1 mm diameter from 24 h cultures, in at least Organisms 3 ml of sterile distilled water. Then, the inoculum was A total of 10 strains were used in the course of this study. suspended by vigorous shaking on a vortex mixer for 15 Six clinical isolates of C. glabrata from Hospital Escala s and the cell density was adjusted to the density of a 0.5 Braga in Portugal were recovered from different sites: oral McFarland standard and adding sterile distilled water as BIOFOULING 571 required,
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